HIF-1α regulates epithelial inflammation by cell autonomous NFκB activation and paracrine stromal remodeling

Blood

Volumn 111, Issue 7, 2008, Pages 3343-3354

  Scortegagna, Marzia ^a   Cataisson, Christophe ^b   Martin, Rebecca J ^a   Hicklin, Daniel J ^c   Schreiber, Robert D ^a,d   Yuspa, Stuart H ^b   Arbeit, Jeffrey M ^a,d  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c ELI LILLY AND COMPANY   (United States)

^d USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHORBOL 13 ACETATE 12 MYRISTATE; PLACENTAL GROWTH FACTOR; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; CARCINOGEN; CYTOKINE; HIF1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; EPITHELIUM; HYPERSENSITIVITY; INFLAMMATION; INFLAMMATORY CELL; KERATINOCYTE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROVOCATION TEST; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STROMA; TISSUE REPAIR; TRANSGENIC MOUSE; ACTIVE TRANSPORT; ANIMAL; CELL NUCLEUS; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; DRUG HYPERSENSITIVITY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SECRETION; STROMA CELL; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CARCINOGENS; CELL NUCLEUS; CYTOKINES; DRUG HYPERSENSITIVITY; EPITHELIUM; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION; KERATINOCYTES; MICE; MICE, TRANSGENIC; PARACRINE COMMUNICATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STROMAL CELLS; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 43549112364     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-10-115758     Document Type: Article

References (49)

1. Karin M, LawrenceT, Nizet V. Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer. Cell. 2006;124:823-835.
2. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6:24-37.
3. Zenz R, Eferl R, Kenner L, et al. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature. 2005; 437:369-375.
4. Sano S, Chan KS, Kira M, et al. Signal transducer and activator of transcription 3 is a key regulator of keratinocyte survival and proliferation following UV irradiation. Cancer Res. 2005;65:5720-5729.
5. Semenza G. Signal transduction to hypoxia- inducible factor 1. Biochem Pharmacol. 2002;64:993-998.
6. Le QT, Denko NC, GiacciaAJ. Hypoxic gene expression and metastasis. Cancer Metastasis Rev. 2004;23:293-310.
7. Masson N, Willam C, Maxwell PH, Pugh CW, Ratcliffe PJ. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 2001;20:5197-5206.
8. Reddy SA, Huang JH, Liao WS. Phosphatidylinositol 3-kinase as a mediator of TNF-induced NF- kappa B activation. J Immunol. 2000;164:1355-1363.
9. Jung Y, Isaacs JS, Lee S, Trepel J, Liu ZG, Neckers L. Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochem J. 2003;370:1011-1017.
10. Jung YJ, Isaacs JS, Lee S, Trepel J, Neckers L. IL-1beta-mediated up-regulation of HIF-1alpha via an NFkappaB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J. 2003;17:2115-2117.
11. Hollander AP, Corke KP, Freemont AJ, Lewis CE. Expression of hypoxia-inducible factor 1alpha by macrophages in the rheumatoid synovium: implications for targeting of therapeutic genes to the inflamed joint. Arthritis Rheum. 2001;44:1540-1544.
12. Cramer T, Yamanishi Y, Clausen BE, et al. HIF- 1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645-657.
13. Lukashev D, Caldwell C, OhtaA, Chen P, Sitkovsky M. Differential regulation of two alternatively spliced isoforms of hypoxia-inducible factor-1 alpha in activated Tlymphocytes. J Biol Chem. 2001;276:48754-48763.
14. Arbeit JM, Munger K, Howley PM, Hanahan D. Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J Virol. 1994;68:4358-4368.
15. Elson DA, Thurston G, Huang LE, et al. Induction of hypervascularity without leak or inflammation in transgenic mice overexpressing hypoxia- inducible factor-1 α. Genes Dev. 2001;15:2520-2532.
16. Lu ZH, Wright JD, Belt B, Cardiff RD, Arbeit JM. Hypoxia-inducible factor-1 facilitates cervical cancer progression in human papillomavirus type 16 transgenic mice. Am J Pathol. 2007;171:667-681.
17. Sheehan KC, Calderon J, Schreiber RD. Generation and characterization of monoclonal antibodies specific forthe human IFN-gamma receptor. J Immunol. 1988;140:4231-4237.
18. Wershil BK, Wang ZS, Gordon JR, Galli SJ. Recruitment of neutrophils during IgE-dependent cutaneous late phase reactions in the mouse is mast cell-dependent: partial inhibition of the reaction with antiserum against tumor necrosis factor-alpha. J Clin Invest. 1991;87:446-453.
19. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS Jr. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol. 1999;19:5785-5799.
20. Dlugosz A, Glick A, Tennenbaum T, Weinberg W, Yuspa S. Isolation and utilization of epidermal keratinocytes for oncogene research. In: Vogt P Verma I eds. Oncogene Techniques. Vol. 254. San Diego CA: Academic Press; 1995:3-20.
21. Jiang BH Zheng JZ Leung SW Roe R Semenza GL. Transactivation and inhibitory domains of hypoxia-inducible factor 1alpha. J Biol Chem. 1997;272:19253-19260.
22. Xia YP, Li B, Hylton D, Detmar M, Yancopoulos GD, Rudge JS. Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis. Blood. 2003;102:161-168.
23. Elder D, Elenitsas R, Jaworsky C, Johnson B. Algorithmic classification of skin disease for differential diagnosis. In: Histopathology of the Skin. New York, NY: Lippincott-Raven; 1997:156-163.
24. Altman EM, Kamino H. Diagnosis: psoriasis or not? What are the clues? Semin Cutan Med Surg. 1999;18:25-35.
25. Cataisson C, Joseloff E, Murillas R, et al. Activation of cutaneous protein kinase C alpha induces keratinocyte apoptosis and intraepidermal inflammation by independent signaling pathways. J Immunol. 2003;171:2703-2713.
26. Bozic CR, Gerard NP, von Uexkull-Guldenband C, et al. The murine interleukin 8 type B receptor homologue and its ligands: expression and biological characterization. J Biol Chem. 1994;269: 29355-29358.
27. Bozic CR, Kolakowski LF Jr, Gerard NP, et al. Expression and biologic characterization of the murine chemokine KC. J Immunol. 1995;154:6048-6057.
28. Lee J, Cacalano G, CameratoT, Toy K, Moore MW, Wood WI. Chemokine binding and activities mediated by the mouse IL-8 receptor. J Immunol. 1995;155:2158-2164.
29. Cataisson C, Pearson AJ, Tsien MZ, et al. CXCR2 ligands and G-CSF mediate PKCalphainduced intraepidermal inflammation. J Clin Invest. 2006;116:2757-2766.
30. Cataisson C, Pearson AJ, Torgerson S, Nedospasov SA, Yuspa SH. Protein kinase C alpha-mediated chemotaxis of neutrophils requires NF- kappa B activity but is independent of TNF alpha signaling in mouse skin in vivo. J Immunol. 2005;174:1686-1692.
31. Hobbs RM, Silva-Vargas V, Groves R, Watt FM. Expression of activated MEK1 in differentiating epidermal cells is sufficient to generate hyperpro- liferative and inflammatory skin lesions. J Invest Dermatol. 2004;123:503-515.
32. Vermeulen L, De Wilde G, Van Damme P, Vanden Berghe W, Haegeman G. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 2003;22:1313-1324.
33. Schmitz ML, Mattioli I, Buss H, Kracht M. NF- kappaB: a multifaceted transcription factor regulated at several levels. Chembiochem. 2004;5:1348-1358.
34. Oura H, Bertoncini J, Velasco P, Brown LF, Carmeliet P, Detmar M. A critical role of placental growth factor in the induction of inflammation and edema formation. Blood. 2003;101:560-567.
35. Kunstfeld R, Hirakawa S, Hong YK, et al. Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-Atransgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood. 2004;104:1048-1057.
36. Walmsley SR, Cadwallader KA, Chilvers ER. The role of HIF-1alpha in myeloid cell inflammation. Trends Immunol. 2005;26:434-439.
37. Walmsley SR, Print C, Farahi N, et al. Hypoxia- induced neutrophil survival is mediated by HIF- 1alpha-dependent NF-kappaB activity. J Exp Med. 2005;201:105-115.
38. Peyssonnaux C, Datta V, Cramer T, et al. HIF- 1alpha expression regulates the bactericidal capacity of phagocytes. J Clin Invest. 2005;115:1806-1815.
39. Digicaylioglu M, Lipton SA. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature. 2001;412:641-647.
40. Dhawan P, Richmond A. Anovel NF-kappa Binducing kinase-MAPK signaling pathway upregulates NF-kappa B activity in melanoma cells. J Biol Chem. 2002;277:7920-7928.
41. Bohuslav J, Chen LF, Kwon H, Mu Y, Greene WC. p53 induces NF-kappaB activation by an IkappaB kinase-independent mechanism involving phos- phorylation of p65 by ribosomal S6 kinase 1. J Biol Chem. 2004;279:26115-26125.
42. Kim KW, Kim SH, Lee EY, et al. Extracellular signal-regulated kinase/90-KDA ribosomal S6 kinase/nuclear factor-kappa B pathway mediates phorbol 12-myristate 13-acetate-induced megakaryocytic differentiation of K562 cells. J Biol Chem. 2001;276:13186-13191.
43. Wang D, Richmond A. Nuclear factor-kappa B activation by the CXC chemokine melanoma growth-stimulatory activity/growth-regulated protein involves the MEKK1/p38 mitogen-activated protein kinase pathway. J Biol Chem. 2001;276:3650-3659.
44. Liu ZG. Molecular mechanism of TNF signaling and beyond. Cell Res. 2005;15:24-27.
45. Tang L, Yu Y, Chen J, Li Q, Yan M, Guo Z. The inhibitory effect of VitD3 on proliferation of keratinocyte cell line HACAT is mediated by downregulation of CXCR2 expression. Clin Exp Dermatol. 2003;28:416-419.
46. Harris AL. Hypoxia: a key regulatory factor in tumor growth. Nat Rev Cancer. 2001;2:38-46.
47. Semenza GL. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol Med. 2002;8(suppl):S62-S67.
48. Zhong H, Chiles K, Feldser D, et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor an- giogenesis and therapeutics. Cancer Res. 2000;60:1541-1545.
49. Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM, Semenza GL. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem. 2002;277:38205-38211.